Interpretive Summary: Excessive use of nitrogen (N), the single most widely used chemical input in agriculture, has potential to contaminate soil and water and release N into atmosphere, thus impacting ecosystems. Alternative sustainable agriculture systems that use leguminous cover crops such as hairy vetch (Vicia villosa Roth) can fix atmospheric N, enrich soil organic matter by fixing carbon, and increase microbial biomass. Because hairy vetch residue is richer in N, plants grown in hairy vetch cover crop mulch in the field generally require half the regular dose of a synthetic fertilizer. Previously, N signaling pathways were found associated with hairy vetch grown tomatoes suggesting that N in hairy vetch residue may be the basis for delayed leaf senescence and disease tolerance of tomato plants grown in legume cover crop. We designed a pot-experiment in the field to analyze growth and gene expression in tomatoes grown in soil overwintered without a cover crop (bare soil) and in soil overwintered with a hairy vetch cover crop including the vetch residue on the soil surface. Additionally, tomatoes were grown in the absence or presence of supplemental N fertilizer to aid distinguishing tomato responses to vetch from those to inorganic nitrogen. Tomatoes responded to soil and residue from a hairy vetch cover crop differently than tomato response to inorganic nitrogen. Tomato fruit production, plant biomass parameters, and photosynthesis were higher in plants grown in vetch than bare soil. Vetch-grown plants prevented a decline in expression of several genes regulating nitrogen and carbon metabolism and enhanced expression of a defense-related gene compared to that seen in tomatoes grown in bare soil. This research provides evidence that the many positive responses of tomatoes to a hairy vetch cover crop observed in the field is mediated by more complex physiological processes than simply the additional N provided by the vetch cover crop. This research will be of interest to basic plant scientists as well as to production specialists and growers interested in adopting sustainable practices.

Technical Abstract:
Tomatoes responded to soil and residue from a hairy vetch cover crop differently on many levels than tomato response to inorganic nitrogen. Tomato fruit production, plant biomass parameters, and photosynthesis were higher in plants grown in vetch than bare soil. Tomato growth and photosynthesis metrics exhibited a parabolic response to inorganic N in bare soil suggesting the potential for N toxicity in pots with the highest N rate. High leaf putrescine levels in these same treatments just prior to fruit ripening confirmed potential biotic stress in these treatments. Vetch grown tomato plants mitigated these effects by maintaining elevated photosynthetic rates and normal putrescine levels at high inorganic N levels. In addition, vetch-grown plants mitigated a decline in expression of several genes regulating nitrogen and carbon metabolism, and led to an upregulation of the defense-related gene, osmotin, relative to plants grown in bare soil. This research provides evidence that the many positive responses of tomatoes to a hairy vetch cover crop observed in the field is mediated by more complex physiological processes than simply the additional N provided by the vetch cover crop.